Are brain networks stable during a 24-hour period?

Despite the widespread view of the brain as a large complex network, the dynamicity of the brain network over the course of a day has yet to be explored. To investigate whether the spontaneous human brain network maintains long-term stability throughout a day, we evaluated the intra-class correlation coefficient (ICC) of results from an independent component analysis (ICA), seed correlation analysis, and graph-theoretical analysis of resting state functional MRI, acquired from 12 young adults at three-hour intervals over 24 consecutive hours. According to the ICC of the usage strength of the independent network component defined by the root mean square of the temporal weights of the network components, the default mode network centered at the posterior cingulate cortex and precuneus, the superior parietal, and secondary motor networks showed a high temporal stability throughout the day (ICC>0.5). However, high intra-individual dynamicity was observed in the default mode network, including the anterior cingulate cortex and medial prefrontal cortex or posterior-anterior cingulate cortex, the hippocampal network, and the parietal and temporal networks. Seed correlation analysis showed a highly stable (ICC>0.5) extent of functionally connected regions from the posterior cingulate cortex, but poor stability from the hippocampus throughout the day. Graph-theoretical analysis using local and global network efficiency suggested that local brain networks are temporally stable but that long-range integration behaves dynamically in the course of a day. These results imply that dynamic network properties are a nature of the resting state brain network, which remains to be further researched.

[1]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[2]  Jeff H. Duyn,et al.  Modulation of spontaneous fMRI activity in human visual cortex by behavioral state , 2009, NeuroImage.

[3]  Wang Zhan,et al.  Group independent component analysis reveals consistent resting-state networks across multiple sessions , 2008, Brain Research.

[4]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[5]  M. Annett A classification of hand preference by association analysis. , 1970, British journal of psychology.

[6]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[7]  Seung-Schik Yoo,et al.  The Unrested Resting Brain: Sleep Deprivation Alters Activity within the Default-mode Network , 2010, Journal of Cognitive Neuroscience.

[8]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[9]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[10]  Vince D. Calhoun,et al.  A method for functional network connectivity among spatially independent resting-state components in schizophrenia , 2008, NeuroImage.

[11]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[12]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[13]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[14]  Edwin M. Robertson,et al.  The Resting Human Brain and Motor Learning , 2009, Current Biology.

[15]  Vince D. Calhoun,et al.  A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data , 2009, NeuroImage.

[16]  N. Zisapel,et al.  Late evening brain activation patterns and their relation to the internal biological time, melatonin, and homeostatic sleep debt , 2009, Human brain mapping.

[17]  O. Dietrich,et al.  Test–retest reproducibility of the default‐mode network in healthy individuals , 2009, Human brain mapping.

[18]  Luciano Mecacci,et al.  Cognitive failures and circadian typology , 2004 .

[19]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[20]  M. Boly,et al.  Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. , 2010, Brain : a journal of neurology.

[21]  Yong He,et al.  Disrupted small-world networks in schizophrenia. , 2008, Brain : a journal of neurology.

[22]  Chunshui Yu,et al.  Whole brain functional connectivity in the early blind. , 2007, Brain : a journal of neurology.

[23]  Steven C. R. Williams,et al.  Measuring fMRI reliability with the intra-class correlation coefficient , 2009, NeuroImage.

[24]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[25]  Xi-Nian Zuo,et al.  Reliable intrinsic connectivity networks: Test–retest evaluation using ICA and dual regression approach , 2010, NeuroImage.

[26]  Matthijs Vink,et al.  Reduced functional coupling in the default‐mode network during self‐referential processing , 2010, Human brain mapping.

[27]  Mark D'Esposito,et al.  Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses , 2004, NeuroImage.

[28]  Edward T. Bullmore,et al.  Reproducibility of graph metrics of human brain functional networks , 2009, NeuroImage.

[29]  Tülay Adali,et al.  Estimating the number of independent components for functional magnetic resonance imaging data , 2007, Human brain mapping.

[30]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

[31]  C. Schmidt,et al.  A time to think: Circadian rhythms in human cognition , 2007, Cognitive neuropsychology.

[32]  Hernando Ombao,et al.  Regional brain glucose metabolism during morning and evening wakefulness in humans: preliminary findings. , 2004, Sleep.

[33]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[34]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[35]  S. Daan,et al.  Timing of human sleep: recovery process gated by a circadian pacemaker. , 1984, The American journal of physiology.

[36]  Olaf Sporns,et al.  The small world of the cerebral cortex , 2007, Neuroinformatics.

[37]  Stephen M. Smith,et al.  Advances and Pitfalls in the Analysis and Interpretation of Resting-State FMRI Data , 2010, Front. Syst. Neurosci..

[38]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Liang Wang,et al.  Altered small‐world brain functional networks in children with attention‐deficit/hyperactivity disorder , 2009, Human brain mapping.

[40]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[41]  A. Braun,et al.  Decoupling of the brain's default mode network during deep sleep , 2009, Proceedings of the National Academy of Sciences.

[42]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[43]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[44]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[45]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[46]  S Makeig,et al.  Blind separation of auditory event-related brain responses into independent components. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[47]  M. Mintun,et al.  The default mode network and self-referential processes in depression , 2009, Proceedings of the National Academy of Sciences.

[48]  Jutta S. Mayer,et al.  Specialization in the default mode: Task‐induced brain deactivations dissociate between visual working memory and attention , 2009, Human brain mapping.

[49]  Russell A. Poldrack,et al.  Long-term test–retest reliability of functional MRI in a classification learning task , 2006, NeuroImage.

[50]  S. Rombouts,et al.  Reduced resting-state brain activity in the "default network" in normal aging. , 2008, Cerebral cortex.

[51]  C. Stam,et al.  Small‐world properties of nonlinear brain activity in schizophrenia , 2009, Human brain mapping.

[52]  W. Revelle,et al.  Impulsivity and time of day: is rate of change in arousal a function of impulsivity? , 1994, Journal of personality and social psychology.

[53]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[54]  Stephen M. Smith,et al.  fMRI resting state networks define distinct modes of long-distance interactions in the human brain , 2006, NeuroImage.

[55]  L. Hasher,et al.  Implicit memory, age, and time of day: paradoxical priming effects. , 2005, Psychological science.

[56]  Gregory G. Brown,et al.  r Human Brain Mapping 29:958–972 (2008) r Test–Retest and Between-Site Reliability in a Multicenter fMRI Study , 2022 .

[57]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[58]  S Makeig,et al.  Analysis of fMRI data by blind separation into independent spatial components , 1998, Human brain mapping.

[59]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[60]  T. Koenig,et al.  Topographic Electrophysiological Signatures of fMRI Resting State Networks , 2010, PloS one.

[61]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[62]  Andrzej Urbanik,et al.  DIURNAL PATTERNS OF ACTIVITY OF THE ORIENTING AND EXECUTIVE ATTENTION NEURONAL NETWORKS IN SUBJECTS PERFORMING A STROOP-LIKE TASK: A FUNCTIONAL MAGNETIC RESONANCE IMAGING STUDY , 2010, Chronobiology international.

[63]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

[64]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[65]  C. J. Honeya,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009 .

[66]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[67]  A. Borbély A two process model of sleep regulation. , 1982, Human neurobiology.

[68]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[69]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[70]  Guang H. Yue,et al.  Reductions in interhemispheric motor cortex functional connectivity after muscle fatigue , 2005, Brain Research.